Inhibiting corticospinal excitability by entraining ongoing mu-alpha rhythm in motor cortex

Sensorimotor mu-alpha rhythm reflects the state of cortical excitability. Repetitive transcranial magnetic stimulation (rTMS) can modulate neural synchrony by inducing periodic electric fields (E-fields) in the cortical networks. We hypothesized that the increased synchronization of mu-alpha rhythm would inhibit the corticospinal excitability reflected by decreased motor evoked potentials (MEP). In seventeen healthy participants, we applied rhythmic, arrhythmic, and sham rTMS over the left M1. The stimulation intensity was individually adapted to 35 mV/mm using prospective E-field estimation. This intensity corresponded to ca. 40% of the resting motor threshold. We found that rhythmic rTMS increased the synchronization of mu-alpha rhythm, increased mu-alpha/beta power, and reduced MEPs. On the other hand, arrhythmic rTMS did not change the ongoing mu-alpha synchronization or MEPs, though it increased the alpha/beta power. We concluded that low intensity, rhythmic rTMS can synchronize mu-alpha rhythm and modulate the corticospinal excitability in M1. Highlights We studied the effect of rhythmic rTMS induced E-field at 35 mV/mm in the M1 Prospective electric field modeling guided the individualized rTMS intensities Rhyhtmic rTMS entrained mu-alpha rhythm and modulated mu-alpha/beta power Arrhythmic rTMS did not synchronize ongoing activity though increased mu-alpha/beta power. Rhythmic but not arrhythmic or sham rTMS inhibited the cortical excitability in M1

[1]  Joachim Gross,et al.  Oscillatory activity reflects the excitability of the human somatosensory system , 2006, NeuroImage.

[2]  S. Tobimatsu,et al.  Prestimulus cortical EEG oscillations can predict the excitability of the primary motor cortex , 2019, Brain Stimulation.

[3]  A. Berardelli,et al.  The prolonged cortical silent period in patients with Huntington's disease , 2001, Clinical Neurophysiology.

[4]  Hartwig R. Siebner,et al.  The non-transcranial TMS-evoked potential is an inherent source of ambiguity in TMS-EEG studies , 2018, NeuroImage.

[5]  Tuo-Hung Hou,et al.  SLIM: Simultaneous Logic-in-Memory Computing Exploiting Bilayer Analog OxRAM Devices , 2018, Scientific Reports.

[6]  B. Christensen,et al.  The effects of repetitive transcranial magnetic stimulation on cortical inhibition in healthy human subjects , 2006, Experimental Brain Research.

[7]  P. Belardinelli,et al.  Nil effects of μ-rhythm phase-dependent burst-rTMS on cortical excitability in humans: A resting-state EEG and TMS-EEG study , 2018, PloS one.

[8]  Arkady Pikovsky,et al.  A universal concept in nonlinear sciences , 2006 .

[9]  A. Berardelli,et al.  Spread of electrical activity at cortical level after repetitive magnetic stimulation in normal subjects , 2002, Experimental Brain Research.

[10]  G. Burnstock,et al.  The expanding field of purinergic signalling , 2009, Trends in Neurosciences.

[11]  Joël M. H. Karel,et al.  Quantifying Neural Oscillatory Synchronization: A Comparison between Spectral Coherence and Phase-Locking Value Approaches , 2016, PloS one.

[12]  Steven H. Strogatz,et al.  Synchronization: A Universal Concept in Nonlinear Sciences , 2003 .

[13]  W. Paulus,et al.  Weak rTMS-induced electric fields produce neural entrainment in humans , 2019, Scientific Reports.

[14]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[15]  C. Schroeder,et al.  Low-frequency neuronal oscillations as instruments of sensory selection , 2009, Trends in Neurosciences.

[16]  Axel Thielscher,et al.  Field modeling for transcranial magnetic stimulation: A useful tool to understand the physiological effects of TMS? , 2015, 2015 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[17]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[18]  Jürgen Kurths,et al.  Synchronization - A Universal Concept in Nonlinear Sciences , 2001, Cambridge Nonlinear Science Series.

[19]  W. Drongelen,et al.  Localization of brain electrical activity via linearly constrained minimum variance spatial filtering , 1997, IEEE Transactions on Biomedical Engineering.

[20]  G. Fuggetta,et al.  Human cortical theta reactivity to high‐frequency repetitive transcranial magnetic stimulation , 2012, Human brain mapping.

[21]  Enea F Pavone,et al.  Acute modulation of cortical oscillatory activities during short trains of high‐frequency repetitive transcranial magnetic stimulation of the human motor cortex: A combined EEG and TMS study , 2008, Human brain mapping.

[22]  Christoph Zrenner,et al.  Real-time EEG-defined excitability states determine efficacy of TMS-induced plasticity in human motor cortex , 2017, Brain Stimulation.

[23]  W. Paulus,et al.  Short-lived Alpha Power Suppression Induced by Low-intensity Arrhythmic rTMS , 2020, Neuroscience.

[24]  Per B. Brockhoff,et al.  lmerTest Package: Tests in Linear Mixed Effects Models , 2017 .

[25]  M. Hallett,et al.  Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. , 1994, Brain : a journal of neurology.

[26]  C. Gerloff,et al.  Inhibitory control of acquired motor programmes in the human brain. , 2002, Brain : a journal of neurology.

[27]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[28]  Á. Pascual-Leone,et al.  Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation , 2000, Clinical Neurophysiology.

[29]  A. van Oosterom,et al.  The potential distribution generated by surface electrodes in inhomogeneous volume conductors of arbitrary shape , 1991, IEEE Transactions on Biomedical Engineering.

[30]  W. Klimesch,et al.  EEG alpha oscillations: The inhibition–timing hypothesis , 2007, Brain Research Reviews.

[31]  W. Paulus,et al.  Selecting stimulation intensity in repetitive transcranial magnetic stimulation studies: A systematic review between 1991 and 2020 , 2020, bioRxiv.

[32]  Christoph Zrenner,et al.  Sensorimotor mu-alpha power is positively related to corticospinal excitability , 2018, Brain Stimulation.

[33]  Markus Zahn,et al.  Three-dimensional head model Simulation of transcranial magnetic stimulation , 2004, IEEE Transactions on Biomedical Engineering.

[34]  S. Jung,et al.  Changes in motor cortical excitability induced by high-frequency repetitive transcranial magnetic stimulation of different stimulation durations , 2008, Clinical Neurophysiology.

[35]  Risto J. Ilmoniemi,et al.  EEG oscillations and magnetically evoked motor potentials reflect motor system excitability in overlapping neuronal populations , 2010, Clinical Neurophysiology.